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      Modeling Human Organ Development and Diseases With Fetal Tissue–Derived Organoids

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          Abstract

          Recent advances in human organoid technology have greatly facilitated the study of organ development and pathology. In most cases, these organoids are derived from either pluripotent stem cells or adult stem cells for the modeling of developmental events and tissue homeostasis. However, due to the lack of human fetal tissue references and research model, it is still challenging to capture early developmental changes and underlying mechanisms in human embryonic development. The establishment of fetal tissue–derived organoids in rigorous time points is necessary. Here we provide an overview of the strategies and applications of fetal tissue–derived organoids, mainly focusing on fetal organ development research, developmental defect disease modeling, and organ–organ interaction study. Discussion of the importance of fetal tissue research also highlights the prospects and challenges in this field.

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          Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche.

          Toshiro Sato, Robert G J Vries, Hugo J. Snippert … (2009)
          The intestinal epithelium is the most rapidly self-renewing tissue in adult mammals. We have recently demonstrated the presence of about six cycling Lgr5(+) stem cells at the bottoms of small-intestinal crypts. Here we describe the establishment of long-term culture conditions under which single crypts undergo multiple crypt fission events, while simultanously generating villus-like epithelial domains in which all differentiated cell types are present. Single sorted Lgr5(+) stem cells can also initiate these cryptvillus organoids. Tracing experiments indicate that the Lgr5(+) stem-cell hierarchy is maintained in organoids. We conclude that intestinal cryptvillus units are self-organizing structures, which can be built from a single stem cell in the absence of a non-epithelial cellular niche.
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            Cerebral organoids model human brain development and microcephaly

            Madeline Lancaster, Magdalena Renner, Carol-Anne Martin … (2013)
            The complexity of the human brain has made it difficult to study many brain disorders in model organisms, and highlights the need for an in vitro model of human brain development. We have developed a human pluripotent stem cell-derived 3D organoid culture system, termed cerebral organoid, which develops various discrete though interdependent brain regions. These include cerebral cortex containing progenitor populations that organize and produce mature cortical neuron subtypes. Furthermore, cerebral organoids recapitulate features of human cortical development, namely characteristic progenitor zone organization with abundant outer radial glial stem cells. Finally, we use RNAi and patient-specific iPS cells to model microcephaly, a disorder that has been difficult to recapitulate in mice. We demonstrate premature neuronal differentiation in patient organoids, a defect that could explain the disease phenotype. Our data demonstrate that 3D organoids can recapitulate development and disease of even this most complex human tissue.
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              Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium.

              Toshiro Sato, Daniel E. Stange, Marc Ferrante … (2011)
              We previously established long-term culture conditions under which single crypts or stem cells derived from mouse small intestine expand over long periods. The expanding crypts undergo multiple crypt fission events, simultaneously generating villus-like epithelial domains that contain all differentiated types of cells. We have adapted the culture conditions to grow similar epithelial organoids from mouse colon and human small intestine and colon. Based on the mouse small intestinal culture system, we optimized the mouse and human colon culture systems. Addition of Wnt3A to the combination of growth factors applied to mouse colon crypts allowed them to expand indefinitely. Addition of nicotinamide, along with a small molecule inhibitor of Alk and an inhibitor of p38, were required for long-term culture of human small intestine and colon tissues. The culture system also allowed growth of mouse Apc-deficient adenomas, human colorectal cancer cells, and human metaplastic epithelia from regions of Barrett's esophagus. We developed a technology that can be used to study infected, inflammatory, or neoplastic tissues from the human gastrointestinal tract. These tools might have applications in regenerative biology through ex vivo expansion of the intestinal epithelia. Studies of these cultures indicate that there is no inherent restriction in the replicative potential of adult stem cells (or a Hayflick limit) ex vivo. Copyright © 2011 AGA Institute. Published by Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Cell Transplant
                Journal ID (iso-abbrev): Cell Transplant
                Journal ID (publisher-id): CLL
                Journal ID (hwp): spcll
                Title: Cell Transplantation
                Publisher: SAGE Publications (Sage CA: Los Angeles, CA )
                ISSN (Print): 0963-6897
                ISSN (Electronic): 1555-3892
                Publication date (Electronic): 19 September 2022
                Publication date Collection: Jan-Dec 2022
                Volume: 31
                Electronic Location Identifier: 09636897221124481
                Affiliations
                [1 ]State Key Laboratory of Genetic Engineering, School of Life Sciences, Zhongshan Hospital, Fudan University, Shanghai, China
                [2 ]bioGenous Biotechnology, Inc., Hangzhou, China
                Author notes
                [*]Bing Zhao, State Key Laboratory of Genetic Engineering, School of Life Sciences, Zhongshan Hospital, Fudan University, Shanghai 200438, China. Email: bingzhao@ 123456fudan.edu.cn
                Author information
                https://orcid.org/0000-0001-9891-3569
                Article
                Publisher ID: 10.1177_09636897221124481
                DOI: 10.1177/09636897221124481
                PMC ID: 9490458
                PubMed ID: 36121224
                SO-VID: a206b2f3-e292-4647-9cfb-1d36e6f1d38f
                Copyright © © The Author(s) 2022
                License:

                This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License ( https://creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages ( https://us.sagepub.com/en-us/nam/open-access-at-sage).

                History
                Date received : 25 May 2022
                Date revision received : 2 August 2022
                Date accepted : 22 August 2022
                Funding
                Funded by: Shanghai Pilot Program for Basic Research - Fudan University 21TQ1400100, ;
                Award ID: 21TQ003
                Funded by: National Key Research and Development Program of China, FundRef https://doi.org/10.13039/501100012166;
                Award ID: 2018YFA0109400
                Funded by: National Natural Science Foundation of China, FundRef https://doi.org/10.13039/501100001809;
                Award ID: 32022022
                Categories
                Subject: Review (Invited)
                Custom metadata
                cover-date January-December 2022
                typesetter ts1

                Keywords: organoids,human fetal tissues,organ development,developmental defect diseases
                Data availability:
                Keywords: organoids, human fetal tissues, organ development, developmental defect diseases

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